Functional analysis of the nifQdctA1y4vGHIJ operon of Sinorhizobium fredii strain NGR234 using a transposon with a NifA-dependent read-out promoter

Microbiology

Volumn 157, Issue 10, 2011, Pages 2745-2758

  Fumeaux, Coralie ^a   Bakkou, Nadia ^a   Kopcińska, Joanna ^b   Golinowski, Wladyslav ^b   Westenberg, David J ^c   Muller, Peter ^d   Perret, Xavier ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^c MISSOURI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (United States)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DNA TRANSPOSITION; DOWNSTREAM PROCESSING; GENE MUTATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; LEGUME; MUTAGENESIS; NIFQDCTA1Y4VGHIJ GENE; NITROGEN FIXATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROMOTER REGION; RHIZOBIACEAE; SINORHIZOBIUM FREDII; TRANSPOSON;

BACTERIAL PROTEINS; BASE SEQUENCE; DICARBOXYLIC ACID TRANSPORTERS; DNA TRANSPOSABLE ELEMENTS; FABACEAE; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; OPERON; PROMOTER REGIONS, GENETIC; SINORHIZOBIUM FREDII; SYMBIOSIS; TRANSCRIPTION FACTORS;

SINORHIZOBIUM FREDII;

EID: 80053449488     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.049999-0     Document Type: Article

References (61)

1. Aneja, P. & Charles, T. C. (2005). Characterization of bdhA, encoding the enzyme D-3-hydroxybutyrate dehydrogenase, from Sinorhizobium sp. strain NGR234. FEMS Microbiol Lett 242, 87-94.
2. Badenoch-Jones, J., Holton, T. A., Morrison, C. M., Scott, K. F. & Shine, J. (1989). Structural and functional analysis of nitrogenase genes from the broad-host-range Rhizobium strain ANU240. Gene 77, 141-153.
3. Broughton, W. J. & Dilworth, M. J. (1971). Control of leghaemoglobin synthesis in snake beans. Biochem J 125, 1075-1080.
4. Broughton, W. J., Wong, C.-H., Lewin, A., Samrey, U., Myint, H., Meyer, z. A. H., Dowling, D. N. & Simon, R. (1986). Identification of Rhizobium plasmid sequences involved in recognition of Psophocarpus, Vigna, and other legumes. J Cell Biol 102, 1173-1182.
5. David, M., Daveran, M. L., Batut, J., Dedieu, A., Domergue, O., Ghai, J., Hertig, C., Boistard, P. & Kahn, D. (1988). Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54, 671-683.
6. Dixon, R. & Kahn, D. (2004). Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2, 621-631.
7. Dombrecht, B., Marchal, K., Vanderleyden, J. & Michiels, J. (2002). Prediction and overview of the RpoN-regulon in closely related species of the Rhizobiales. Genome Biol 3, RESEARCH0076.
8. Fellay, R., Hanin, M., Montorzi, G., Frey, J., Freiberg, C., Golinowski, W., Staehelin, C., Broughton, W. J. & Jabbouri, S. (1998). nodD2 of Rhizobium sp. NGR234 is involved in the repression of the nodABC operon. Mol Microbiol 27, 1039-1050.
9. Figurski, D. H. & Helinski, D. R. (1979). Replication of an origincontaining derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76, 1648-1652.
10. Fischer, H. M. (1994). Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58, 352-386.
11. Fischer, H. M., Alvarez-Morales, A. & Hennecke, H. (1986). The pleiotropic nature of symbiotic regulatory mutants: Bradyrhizobium japonicum nifA gene is involved in control of nif gene expression and formation of determinate symbiosis. EMBO J 5, 1165-1173.
12. Freiberg, C., Fellay, R., Bairoch, A., Broughton, W. J., Rosenthal, A. & Perret, X. (1997). Molecular basis of symbiosis between Rhizobium and legumes. Nature 387, 394-401.
13. Gage, D. J. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68, 280-300.
14. Gibson, K. E., Kobayashi, H. & Walker, G. C. (2008). Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42, 413-441.
15. Golinowski, W., Kopcińska, J. & Borucki, W. (1987). The morphogenesis of lupine root nodules during infection by Rhizobium lupini. Acta Soc Bot Pol 56, 687-703.
16. Hernandez, J. A., Curatti, L., Aznar, C. P., Perova, Z., Britt, R. D. & Rubio, L. M. (2008). Metal trafficking for nitrogen fixation: NifQ donates molybdenum to NifEN/NifH for the biosynthesis of the nitrogenase FeMo-cofactor. Proc Natl Acad Sci U S A 105, 11679-11684.
17. Hirsch, A. M. & Smith, C. A. (1987). Effects of Rhizobium meliloti nif and fix mutants on alfalfa root nodule development. J Bacteriol 169, 1137-1146.
18. Imperial, J., Ugalde, R. A., Shah, V. K. & Brill, W. J. (1984). Role of the nifQ gene product in the incorporation of molybdenum into nitrogenase in Klebsiella pneumoniae. J Bacteriol 158, 187-194.
19. Jefferson, R. A., Burgess, S. M. & Hirsh, D. (1986). b-Glucuronidase from Escherichia coli as a gene-fusion marker. Proc Natl Acad Sci U S A 83, 8447-8451.
20. Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., Watanabe, A., Idesawa, K., Ishikawa, A. & other authors (2000). Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7, 331-338.
21. Keister, D. L., Tully, R. E. & Van Berkum, P. (1999). A cytochrome P450 gene cluster in the Rhizobiaceae. J Gen Appl Microbiol 45, 301-303.
22. Kim, C.-H., Helinski, D. R. & Ditta, G. (1986). Overlapping transcription of the nifA regulatory gene in Rhizobium meliloti. Gene 50, 141-148.
23. Kobayashi, H., Naciri-Graven, Y., Broughton, W. J. & Perret, X. (2004). Flavonoids induce temporal shifts in gene-expression of nodbox controlled loci in Rhizobium sp. NGR234. Mol Microbiol 51, 335-347.
24. Labes, M., Rastogi, V., Watson, R. & Finan, T. M. (1993). Symbiotic nitrogen fixation by a nifA deletion mutant of Rhizobium meliloti: the role of an unusual ntrC allele. J Bacteriol 175, 2662-2673.
25. Lewin, A., Cervantes, E., Chee-Hoong, W. & Broughton, W. J. (1990). nodSU, two new nod genes of the broad host range Rhizobium strain NGR234 encode host-specific nodulation of the tropical tree Leucaena leucocephala. Mol Plant Microbe Interact 3, 317-326.
26. Lopez, O., Morera, C., Miranda-Rios, J., Girard, L., Romero, D. & Soberón, M. (2001). Regulation of gene expression in response to oxygen in Rhizobium etli: role of FnrN in fixNOQP expression and in symbiotic nitrogen fixation. J Bacteriol 183, 6999-7006.
27. Luyten, E., Swinnen, E., Vlassak, K., Verreth, C., Dombrecht, B. & Vanderleyden, J. (2001). Analysis of a symbiosis-specific cytochrome P450 homolog in Rhizobium sp. BR816. Mol Plant Microbe Interact 14, 918-924.
28. Marie, C., Deakin, W. J., Viprey, V., Kopcińska, J., Golinowski, W., Krishnan, H. B., Perret, X. & Broughton, W. J. (2003). Characterization of Nops, nodulation outer proteins, secreted via the type III secretion system of NGR234. Mol Plant Microbe Interact 16, 743-751.
29. Masson-Boivin, C., Giraud, E., Perret, X. & Batut, J. (2009). Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17, 458-466.
30. Mergaert, P., Uchiumi, T., Alunni, B., Evanno, G., Cheron, A., Catrice, O., Mausset, A. E., Barloy-Hubler, F., Galibert, F. & other authors (2006). Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci U S A 103, 5230-5235.
31. Moreno-Vivian, C., Hennecke, S., Puhler, A. & Klipp, W. (1989). Open reading frame 5 (ORF5), encoding a ferredoxinlike protein, and nifQ are cotranscribed with nifE, nifN, nifX, and ORF4 in Rhodobacter capsulatus. J Bacteriol 171, 2591-2598.
32. Muller, P. (2004). Use of the multipurpose transposon TnKPK2 for the mutational analysis of chromosomal regions upstream and downstream of the sipF gene in Bradyrhizobium japonicum. Mol Genet Genomics 271, 359-366.
33. Muller, J., Wiemken, A. & Boller, T. (2001). Redifferentiation of bacteria isolated from Lotus japonicus root nodules colonized by Rhizobium sp. NGR234. J Exp Bot 52, 2181-2186.
34. Oldroyd, G. E. & Downie, J. A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59, 519-546.
35. Østerås, M., Finan, T. M. & Stanley, J. (1991). Site-directed mutagenesis and DNA sequence of pckA of Rhizobium NGR234, encoding phosphoenolpyruvate carboxykinase: gluconeogenesis and host-dependent symbiotic phenotype. Mol Gen Genet 230, 257-269.
36. Perret, X., Broughton, W. J. & Brenner, S. (1991). Canonical ordered cosmid library of the symbiotic plasmid of Rhizobium species NGR234. Proc Natl Acad Sci U S A 88, 1923-1927.
37. Perret, X., Freiberg, C., Rosenthal, A., Broughton, W. J. & Fellay, R. (1999). High-resolution transcriptional analysis of the symbiotic plasmid of Rhizobium sp. NGR234. Mol Microbiol 32, 415-425.
38. Perret, X., Staehelin, C. & Broughton, W. J. (2000). Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64, 180-201.
39. Perret, X., Kobayashi, H. & Collado-Vides, J. (2003). Regulation of expression of symbiotic genes in Rhizobium sp. NGR234. Indian J Exp Biol 41, 1101-1113.
40. Prentki, P. & Krisch, H. M. (1984). In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29, 303-313.
41. Pueppke, S. G. & Broughton, W. J. (1999). Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant Microbe Interact 12, 293-318.
42. Quandt, J. & Hynes, M. F. (1993). Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127, 15-21.
43. Relí, B., Talmont, F., Kopcińska, J., Golinowski, W., Promé, J. C. & Broughton, W. J. (1993). Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Mol Plant Microbe Interact 6, 764-774.
44. Rodríguez-Quiñones, F., Bosch, R. & Imperial, J. (1993). Expression of the nifBfdxNnifOQ region of Azotobacter vinelandii and its role in nitrogenase activity. J Bacteriol 175, 2926-2935.
45. Rosander, A., Frykberg, L., Ausmees, N. & Muller, P. (2003). Identification of extracytoplasmic proteins in Bradyrhizobium japonicum using phage display. Mol Plant Microbe Interact 16, 727-737.
46. Roth, L. E., Jeon, K. W. & Stacey, G. (1988). Homology in endosymbiotic systems: the term 'symbiosome'. In Molecular Genetics of Plant-Microbe Interactions, pp. 220-225. Edited by D. P. S. Verma & R. Palacios. St Paul, Minnesota: APS Press.
47. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor University.
48. Schmeisser, C., Liesegang, H., Krysciak, D., Bakkou, N., Le Quéré, A., Wollherr, A., Heinemeyer, I., Morgenstern, B., Pommerening-Roser, A. & other authors (2009). Rhizobium sp. strain NGR234 possesses a remarkable number of secretion systems. Appl Environ Microbiol 75, 4035-4045.
49. Stanley, J., Dowling, D. N. & Broughton, W. J. (1988). Cloning of hemA from Rhizobium sp. NGR234 and symbiotic phenotype of a gene-directed mutant in diverse legume genera. Mol Gen Genet 215, 32-37.
50. Stanley, J., van Slooten, J. C., Dowling, D. N., Finan, T. M. & Broughton, W. J. (1989). Molecular cloning of the ntrA gene of the broad host-range Rhizobium sp. NGR234, and phenotypes of a site directed mutant. Mol Gen Genet 217, 528-532.
51. Sullivan, J. T., Trzebiatowski, J. R., Cruickshank, R. W., Gouzy, J., Brown, S. D., Elliot, R. M., Fleetwood, D. J., McCallum, N. G., Rossbach, U. & other authors (2002). Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 184, 3086-3095.
52. Trainer, M. A. & Charles, T. C. (2006). The role of PHB metabolism in the symbiosis of rhizobia with legumes. Appl Microbiol Biotechnol 71, 377-386.
53. Trinick, M. J. (1980). Relationships amongst the fast-growing rhizobia of Lablab purpureus, Leucaena leucocephala, Mimosa spp., Acacia farnesiana and Sesbania grandiflora and their affinities with other rhizobial groups. J Appl Bact 49, 39-53.
54. Tully, R. E. & Keister, D. L. (1993). Cloning and mutagenesis of a cytochrome P-450 locus from Bradyrhizobium japonicum that is expressed anaerobically and symbiotically. Appl Environ Microbiol 59, 4136-4142.
55. Tully, R. E., van Berkum, P., Lovins, K. W. & Keister, D. L. (1998). Identification and sequencing of a cytochrome P450 gene cluster from Bradyrhizobium japonicum. Biochim Biophys Acta 1398, 243-255.
56. Van de Velde, W., Zehirov, G., Szatmari, A., Debreczeny, M., Ishihara, H., Kevei, Z., Farkas, A., Mikulass, K., Nagy, A. & other authors (2010). Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327, 1122-1126.
57. Van den Eede, G., Deblaere, R., Goethals, K., Van Montagu, M. & Holsters, M. (1992). Broad host range and promoter selection vectors for bacteria that interact with plants. Mol Plant Microbe Interact 5, 228-234.
58. van Slooten, J. C., Cervantes, E., Broughton, W. J., Wong, C. H. & Stanley, J. (1990). Sequence and analysis of the rpoN sigma factor gene of Rhizobium sp. strain NGR234, a primary coregulator of symbiosis. J Bacteriol 172, 5563-5574.
59. van Slooten, J. C., Bhuvanasvari, T. V., Bardin, S. & Stanley, J. (1992). Two C4-dicarboxylate transport systems in Rhizobium sp. NGR234: rhizobial dicarboxylate transport is essential for nitrogen fixation in tropical legume symbioses. Mol Plant Microbe Interact 5, 179-186.
60. Viprey, V., Del Greco, A., Golinowski, W., Broughton, W. J. & Perret, X. (1998). Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol Microbiol 28, 1381-1389.
61. Yurgel, S. N. & Kahn, M. L. (2004). Dicarboxylate transport by rhizobia. FEMS Microbiol Rev 28, 489-501.